Bone tissue regeneration by 58S bioactive glass scaffolds containing exosome: an in vivo study.
Bioactive glass scaffold
Bone tissue engineering
Exosome
Human endometrial mesenchymal stem cells
Journal
Cell and tissue banking
ISSN: 1573-6814
Titre abrégé: Cell Tissue Bank
Pays: Netherlands
ID NLM: 100965121
Informations de publication
Date de publication:
30 Dec 2023
30 Dec 2023
Historique:
received:
07
06
2023
accepted:
14
11
2023
medline:
2
1
2024
pubmed:
2
1
2024
entrez:
30
12
2023
Statut:
aheadofprint
Résumé
Exosomes, the naturally secreted nanocarriers of cells, have recently been demonstrated to have therapeutic benefits in a variety of disease models where parent cells are not present. However, the use of exosomes in bone defect regeneration has been unusual, and little is documented about the underlying processes. In recent study we produced and characterized exosomes derived human endometrial mesenchymal stem stromal cells and 58S bioactive glass scaffolds; in following, in this research exosome loaded scaffolds synthetized and release of exosome, porosity and bioactivity of them were assessed. More over the effect of scaffolds on repair of critical-size bone defects in rat's calvaria was evaluated by histological examination and micro computed tomography (µ CT). The findings confirmed that constructed porous scaffolds consistently release exosomes; additionally, in vivo findings including Hematoxilin & Eosin staining, Immunohistochemistry, Masson's trichrome, histomorphometric analysis, and µ CT clarified that our implant has osteogenic properties. We discovered that Exo-treated scaffolds might promote osteogenesis especially compared to pure scaffolds, indicating that produced scaffolds containing exosomes could be a potential replacement in bone tissue engineering.
Identifiants
pubmed: 38159136
doi: 10.1007/s10561-023-10120-1
pii: 10.1007/s10561-023-10120-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Amini AR, Laurencin CT, Nukavarapu SP (2012) Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng 40:363–408. https://doi.org/10.1615/CritRevBiomedEng.v40.i5.10
doi: 10.1615/CritRevBiomedEng.v40.i5.10
pubmed: 23339648
pmcid: 3766369
Bellei B, Migliano E, Tedesco M, Caputo S, Papaccio F, Lopez G, Picardo M (2018) Adipose tissue-derived extracellular fraction characterization: Biological and clinical considerations in regenerative medicine. Stem Cell Res Ther 9:1–18. https://doi.org/10.1186/S13287-018-0956-4/FIGURES/8
doi: 10.1186/S13287-018-0956-4/FIGURES/8
Bellucci D, Cannillo V, Sola A (2010) A new bioactive glass composition for bioceramic scaffolds. J Ceram Sci Technol 1:33–40. https://doi.org/10.4416/JCST2010-00008
doi: 10.4416/JCST2010-00008
Bijonowski BM, Yuan X, Jeske R, Li Y, Grant SC (2020) Cyclical aggregation extends in vitro expansion potential of human mesenchymal stem cells. Sci Rep 10:20448. https://doi.org/10.1038/s41598-020-77288-4
doi: 10.1038/s41598-020-77288-4
pubmed: 33235227
pmcid: 7686385
Billström GH, Blom AW, Larsson S, Beswick AD (2013) Application of scaffolds for bone regeneration strategies: current trends and future directions. Injury 1:S28-33. https://doi.org/10.1016/S0020-1383(13)70007-X
doi: 10.1016/S0020-1383(13)70007-X
Boccardi E, Philippart A, Melli V, Altomare L, De Nardo L, Novajra G, Vitale-Brovarone C, Fey T, Boccaccini AR (2016) Bioactivity and mechanical stability of 45S5 bioactive glass scaffolds based on natural marine sponges. Ann Biomed Eng 44(6):1881–1893. https://doi.org/10.1007/s10439-016-1595-5
doi: 10.1007/s10439-016-1595-5
pubmed: 27034242
Brennan M, Layrolle P, Mooney DJ (2020) Biomaterials functionalized with MSC secreted extracellular vesicles and soluble factors for tissue regeneration. Adv Funct Mater 30:1909125. https://doi.org/10.1002/adfm.201909125
doi: 10.1002/adfm.201909125
pubmed: 32952493
pmcid: 7494127
Cooper DR, Wang C, Patel R, Trujillo A, Patel NA, Prather J, Gould LJ, Wu MH (2018) Human adipose-derived stem cell conditioned media and exosomes containing MALAT1 promote human dermal fibroblast migration and ischemic wound healing. Adv Wound Care 7:299–306. https://doi.org/10.1089/wound.2017.0775
doi: 10.1089/wound.2017.0775
Cooper LF, Ravindran S, Huang CC, Kang M (2020) A Role for exosomes in craniofacial tissue engineering and regeneration. Front Physiol 10:1569. https://doi.org/10.3389/fphys.2019.01569
doi: 10.3389/fphys.2019.01569
pubmed: 32009978
pmcid: 6971208
D’Amelio P (2009) Clinical Reviews in Bone and Mineral Metabolism: Introduction. Clin Rev Bone Miner Metab
Dalirfardouei R, Jamialahmadi K, Jafarian AH, Mahdipour E (2019) Promising effects of exosomes isolated from menstrual blood-derived mesenchymal stem cell on wound-healing process in diabetic mouse model. J Tissue Eng Regen Med 13:555–568. https://doi.org/10.1002/term.2799
doi: 10.1002/term.2799
pubmed: 30656863
DiPietro LA (2016) Angiogenesis and wound repair: when enough is enough. J Leukoc Biol 100:979–984. https://doi.org/10.1189/jlb.4mr0316-102r
doi: 10.1189/jlb.4mr0316-102r
pubmed: 27406995
pmcid: 6608066
Ebrahimi-Barough S, Kouchesfahani HM, Ai J, Massumi M (2013) Differentiation of human endometrial stromal cells into oligodendrocyte progenitor cells (OPCs). J Mol Neurosci 51:265–273. https://doi.org/10.1007/s12031-013-9957-z
doi: 10.1007/s12031-013-9957-z
pubmed: 23338937
Farzin A, Hassan S, Ebrahimi-Barough S, Ai A, Hasanzadeh E, Goodarzi A, Ai J (2019) A facile two step heat treatment strategy for development of bioceramic scaffolds for hard tissue engineering applications. Mater Sci Eng C 105:110009. https://doi.org/10.1016/j.msec.2019.110009
doi: 10.1016/j.msec.2019.110009
Fu Q, Saiz E, Rahaman MN, Tomsia AP (2011) Bioactive glass scaffolds for bone tissue engineering: State of the art and future perspectives. Mater Sci Eng C 31:1245–1256. https://doi.org/10.1016/j.msec.2011.04.022
doi: 10.1016/j.msec.2011.04.022
Griffin KS, Davis KM, McKinley TO, Anglen JO, Chu TMG, Boerckel JD, Kacena MA (2015) Evolution of bone grafting: bone grafts and tissue engineering strategies for vascularized bone regeneration. Clin Rev Bone Miner Metab 13:232–244. https://doi.org/10.1007/S12018-015-9194-9
doi: 10.1007/S12018-015-9194-9
Han Y, Li X, Zhang Y, Han Y, Chang F, Ding J (2019) Mesenchymal stem cells for regenerative medicine. Cells 8:886. https://doi.org/10.3390/cells8080886
doi: 10.3390/cells8080886
pubmed: 31412678
pmcid: 6721852
Harrison RH, St-Pierre JP, Stevens MM (2014) Tissue engineering and regenerative medicine: a year in review. Tissue Eng. - Part B Rev 20:1–16. https://doi.org/10.1089/ten.TEB.2013.0668
doi: 10.1089/ten.TEB.2013.0668
pubmed: 24410501
Hasanzadeh E, Mahmoodi N, Basiri A, Esmaeili Ranjbar F, Hassannejad Z, Ebrahimi-Barough S, Azami M, Ai J, Rahimi-Movaghar V (2020) Proanthocyanidin as a crosslinking agent for fibrin, collagen hydrogels and their composites with decellularized Wharton’s-jelly-extract for tissue engineering applications. J Bioact Compat Polym. https://doi.org/10.1177/0883911520956252
Hasanzadeh E, Ebrahimi-Barough S, Mahmoodi N, Mellati A, Nekounam H, Basiri A, Asadpour S, Ghasemi D, Ai J (2021) Defining the role of 17β-estradiol in human endometrial stem cells differentiation into neuron-like cells. Cell Biol Int 45:140–153. https://doi.org/10.1002/cbin.11478
doi: 10.1002/cbin.11478
pubmed: 33049079
He X, Liu Y, Yuan X, Lu L (2014) Enhanced healing of rat calvarial defects with MSCs loaded on BMP-2 releasing chitosan/alginate/hydroxyapatite scaffolds. PLoS ONE 9:e104061. https://doi.org/10.1371/journal.pone.0104061
doi: 10.1371/journal.pone.0104061
pubmed: 25084008
pmcid: 4118996
Ikegame M, Ejiri S, Okamura H (2019) Expression of non-collagenous bone matrix proteins in osteoblasts stimulated by mechanical stretching in the cranial suture of neonatal mice. J Histochem Cytochem 67:107–116. https://doi.org/10.1369/0022155418793588
doi: 10.1369/0022155418793588
pubmed: 30113872
Jung S, Panchalingam KM, Rosenberg L, Behie LA (2012) Ex vivo expansion of human mesenchymal stem cells in defined serum-free media. Stem Cell Int 1:123030. https://doi.org/10.1155/2012/123030
doi: 10.1155/2012/123030
Kangari P, Talaei-Khozani T, Razeghian-Jahromi I, Razmkhah M (2020) Mesenchymal stem cells: amazing remedies for bone and cartilage defects. Stem Cell Res Ther 11:492. https://doi.org/10.1186/s13287-020-02001-1
doi: 10.1186/s13287-020-02001-1
pubmed: 33225992
pmcid: 7681994
Lamichhane TN, Sokic S, Schardt JS, Raiker RS, Lin JW, Jay SM (2015) Emerging roles for extracellular vesicles in tissue engineering and regenerative medicine. Tissue Eng - Part B Rev 21:45–54. https://doi.org/10.1089/ten.teb.2014.0300
doi: 10.1089/ten.teb.2014.0300
pubmed: 24957510
Lan Y, Jin Q, Xie H, Yan C, Ye Y, Zhao X, Chen Z, Xie Z (2020) Exosomes enhance adhesion and osteogenic differentiation of initial bone marrow stem cells on titanium surfaces. Front Cell Dev Biol 1:1. https://doi.org/10.3389/fcell.2020.583234
doi: 10.3389/fcell.2020.583234
Li M, Jiang Y, Hou Q, Zhao Y, Zhong L, Fu X (2022) Potential pre-activation strategies for improving therapeutic efficacy of mesenchymal stem cells: current status and future prospects. Stem Cell Res Ther 13:146: https://doi.org/10.1186/s13287-022-02822-2 .
Liu A, Lin D, Zhao H, Chen L, Cai B, Lin K, Shen SG (2021) Optimized BMSC-derived osteoinductive exosomes immobilized in hierarchical scaffold via lyophilization for bone repair through Bmpr2/Acvr2b competitive receptor-activated Smad pathway. Biomaterials 272:120718. https://doi.org/10.1016/j.biomaterials.2021.120718
doi: 10.1016/j.biomaterials.2021.120718
pubmed: 33838528
Liu Y, Lim J, Teoh SH (2013) Review: Development of clinically relevant scaffolds for vascularised bone tissue engineering. Biotechnol Adv 31:688–705. https://doi.org/10.1016/j.biotechadv.2012.10.003
doi: 10.1016/j.biotechadv.2012.10.003
pubmed: 23142624
Lu Y, Mai Z, Cui L (2023) Zhao X (2023) Engineering exosomes and biomaterial-assisted exosomes as therapeutic carriers for bone regeneration. Stem Cell Res Ther 141(14):1–19. https://doi.org/10.1186/S13287-023-03275-X
doi: 10.1186/S13287-023-03275-X
Lv K, Li Q, Zhang L, Wang Y, Zhong Z, Zhao J, Lin X, Wang J, Zhu K, Xiao C, Ke C, Zhong S, Wu X, Chen J, Yu H, Zhu W, Li X, Wang B, Tang R, Wang J, Huang J, Hu X (2019) Incorporation of small extracellular vesicles in sodium alginate hydrogel as a novel therapeutic strategy for myocardial infarction. Theranostics 9:7403–7416. https://doi.org/10.7150/thno.32637
doi: 10.7150/thno.32637
pubmed: 31695776
pmcid: 6831299
Marolt Presen D, Traweger A, Gimona M, Redl H (2019) Mesenchymal stromal cell-based bone regeneration therapies: from cell transplantation and tissue engineering to therapeutic secretomes and extracellular vesicles. Front Bioeng Biotechnol 27:352. https://doi.org/10.3389/fbioe.2019.00352
doi: 10.3389/fbioe.2019.00352
Marote A, Teixeira FG, Mendes-Pinheiro B, Salgado AJ (2016) MSCs-derived exosomes: cell-secreted nanovesicles with regenerative potential. Front Pharmacol 7:231. https://doi.org/10.3389/fphar.2016.00231
doi: 10.3389/fphar.2016.00231
pubmed: 27536241
pmcid: 4971062
Neri S (2019) Genetic stability of mesenchymal stromal cells for regenerative medicine applications: a fundamental biosafety aspect. Int J Mol Sci 20:2406. https://doi.org/10.3390/ijms20102406
doi: 10.3390/ijms20102406
pubmed: 31096604
pmcid: 6566307
Nooshabadi VT, Khanmohamadi M, Valipour E, Mahdipour S, Salati A, Malekshahi ZV, Shafei S, Amini E, Farzamfar S, Ai J (2020) Impact of exosome-loaded chitosan hydrogel in wound repair and layered dermal reconstitution in mice animal model. 149J Biomed Mater Res - Part A 108:2138-2. https://doi.org/10.1002/jbm.a.36959
Pereira MM, Clark AE, Hench LL (1994) Calcium phosphate formation on sol-gel-derived bioactive glasses in vitro. J Biomed Mater Res 28:693–698. https://doi.org/10.1002/jbm.820280606
doi: 10.1002/jbm.820280606
pubmed: 8071380
Perez JR, Kouroupis D, Li DJ, Best TM, Kaplan L, Correa D (2018) Tissue engineering and cell-based therapies for fractures and bone defects. Front. Bioeng. Biotechnol 31:105. https://doi.org/10.3389/fbioe.2018.00105
doi: 10.3389/fbioe.2018.00105
Ranjbar FE, Foroutan F, Hajian M, Ai J, Farsinejad A, Ebrahimi-Barough S, Dehghan MM, Azami M (2021) Preparation and characterization of 58S bioactive glass based scaffold with Kaempferol-containing Zein coating for bone tissue engineering. J Biomed Mater Res - Part B Appl Biomater 109:1259–1270. https://doi.org/10.1002/jbm.b.34786
doi: 10.1002/jbm.b.34786
Ren S, Lin Y, Liu W, Yang L, Zhao M (2023) MSC-Exos: Important active factor of bone regeneration. Front Bioeng Biotechnol 11:1136453. https://doi.org/10.3389/fbioe.2023.1136453
doi: 10.3389/fbioe.2023.1136453
pubmed: 36814713
pmcid: 9939647
Ronca D, Langella F, Chierchia M, D’Amora U, Russo T, Domingos M, Gloria A, Bartolo P, Ambrosio L (2016) Bone tissue engineering: 3D PCL-based nanocomposite scaffolds with tailored properties. Procedia CIRP 49:51–54. https://doi.org/10.1016/j.procir.2015.07.028
doi: 10.1016/j.procir.2015.07.028
Sepulveda P, Jones JR, Hench LL (2001) Characterization of melt-derived 45S5 and sol-gel-derived 58S bioactive glasses. J Biomed Mater Res 58(6):734–740. https://doi.org/10.1002/jbm.10026
doi: 10.1002/jbm.10026
pubmed: 11745528
Shafei S, Khanmohammadi M, Heidari R, Ghanbari H, Taghdiri Nooshabadi V, Farzamfar S, Akbariqomi M, Sanikhani NS, Absalan M, Tavoosidana G (2020) Exosome loaded alginate hydrogel promotes tissue regeneration in full-thickness skin wounds: an in vivo study. J Biomed Mater Res - Part A 108:545–556. https://doi.org/10.1002/jbm.a.36835
doi: 10.1002/jbm.a.36835
Squillaro T, Peluso G, Galderisi U (2016) Clinical trials with mesenchymal stem cells: an update. Cell Transplant 25:1. https://doi.org/10.3727/096368915X689622
doi: 10.3727/096368915X689622
Stanovici J, Le Nail LR, Brennan MA, Vidal L, Trichet V, Rosset P, Layrolle P (2016) Bone regeneration strategies with bone marrow stromal cells in orthopaedic surgery. Curr Res Transl Med 64:83–90. https://doi.org/10.1016/j.retram.2016.04.006
doi: 10.1016/j.retram.2016.04.006
pubmed: 27316391
Taghian Dehaghani M, Ahmadian M, Fathi M (2015) Synthesis, characterization, and bioactivity evaluation of amorphous and crystallized 58S bioglass nanopowders. Int J Appl Ceram Technol 64:83–90. https://doi.org/10.1111/ijac.12293
doi: 10.1111/ijac.12293
Tavakolizadeh A, Ahmadian M, Fathi MH, Doostmohammadi A, Seyedjafari E, Ardeshirylajimi A (2017) Investigation of osteoinductive effects of different compositions of bioactive glass nanoparticles for bone tissue engineering. ASAIO J. https://doi.org/10.1097/MAT.0000000000000509
doi: 10.1097/MAT.0000000000000509
pubmed: 28033183
Tu J, Wang H, Li H, Dai K, Wang J, Zhang X (2009) The in vivo bone formation by mesenchymal stem cells in zein scaffolds. Biomaterials 30:4369–4376. https://doi.org/10.1016/j.biomaterials.2009.04.054
doi: 10.1016/j.biomaterials.2009.04.054
pubmed: 19539987
Velasco MA, Narváez-Tovar CA, Garzón-Alvarado DA (2015) Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. Biomed Res Int 1:729076. https://doi.org/10.1155/2015/729076
doi: 10.1155/2015/729076
Wang X, Omar O, Vazirisani F, Thomsen P, Ekström K (2018) Mesenchymal stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation. PLoS ONE 13:e0193059. https://doi.org/10.1371/journal.pone.0193059
doi: 10.1371/journal.pone.0193059
pubmed: 29447276
pmcid: 5814093
Wei Y, Tang C, Zhang J, Li Z, Zhang X, Miron RJ, Zhang Y (2019) Extracellular vesicles derived from the mid-to-late stage of osteoblast differentiation markedly enhance osteogenesis in vitro and in vivo. Biochem Biophys Res Commun 514:252–258. https://doi.org/10.1016/j.bbrc.2019.04.029
doi: 10.1016/j.bbrc.2019.04.029
pubmed: 31029430
Wu J, Chen L, Wang R, Song Z, Shen Z, Zhao Y, Huang S, Lin Z (2019a) Exosomes secreted by stem cells from human exfoliated deciduous teeth promote alveolar bone defect repair through the regulation of angiogenesis and osteogenesis. ACS Biomater Sci Eng 5:3561–3571. https://doi.org/10.1021/ACSBIOMATERIALS.9B00607/ASSET/IMAGES/MEDIUM/AB-2019-006074_0006.GIF
doi: 10.1021/ACSBIOMATERIALS.9B00607/ASSET/IMAGES/MEDIUM/AB-2019-006074_0006.GIF
pubmed: 33405738
Wu J, Chen L, Wang R, Song Z, Shen Z, Zhao Y, Huang S, Lin Z (2019b) Exosomes secreted by stem cells from human exfoliated deciduous teeth promote alveolar bone defect repair through the regulation of angiogenesis and osteogenesis. ACS Biomater Sci Eng 1:1. https://doi.org/10.1021/acsbiomaterials.9b00607
doi: 10.1021/acsbiomaterials.9b00607
Wu S, Liu X, Yeung KWK, Liu C, Yang X (2014) Biomimetic porous scaffolds for bone tissue engineering. Mater Sci Eng R Reports 80:1–36. https://doi.org/10.1016/j.mser.2014.04.001
doi: 10.1016/j.mser.2014.04.001
Yang Z, Yang Y, Xu Y, Jiang W, Shao Y, Xing J, Chen Y, Han Y (2021) Biomimetic nerve guidance conduit containing engineered exosomes of adipose-derived stem cells promotes peripheral nerve regeneration. Stem Cell Res Ther 12:442. https://doi.org/10.1186/s13287-021-02528-x
doi: 10.1186/s13287-021-02528-x
pubmed: 34362437
pmcid: 8343914
Zahiri M, Khanmohammadi M, Goodarzi A, Ababzadeh S, Sagharjoghi Farahani M, Mohandesnezhad S, Bahrami N, Nabipour I, Ai J (2020) Encapsulation of curcumin loaded chitosan nanoparticle within poly (ε-caprolactone) and gelatin fiber mat for wound healing and layered dermal reconstitution. Int J Biol Macromol 153:1241–1250. https://doi.org/10.1016/j.ijbiomac.2019.10.255
doi: 10.1016/j.ijbiomac.2019.10.255
pubmed: 31759002
Zhang J, Liu X, Li H, Chen C, Hu B, Niu X, Li Q, Zhao B, Xie Z, Wang Y (2016) Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res Ther 7:136. https://doi.org/10.1186/s13287-016-0391-3
doi: 10.1186/s13287-016-0391-3
pubmed: 27650895
pmcid: 5028974